Increased habitat fragmentation, global warming and other human activities have caused a rise in the frequency of wildfires worldwide. To reduce the risks of uncontrollable fires, prescribed burns are generally conducted during the colder months of the year, a time when in many mammals torpor is expressed regularly. Torpor is crucial for energy conservation, but the low body temperatures (T b) are associated with a decreased responsiveness and torpid animals might therefore face an increased mortality risk during fires. We tested whether hibernators in deep torpor (a) can respond to the smell of smoke and (b) can climb to avoid fires at T bs below normothermic levels. Our data show that torpid eastern pygmy-possums (Cercartetus nanus) are able to detect smoke and also can climb. All males aroused from torpor when the smoke stimulus was presented at an ambient temperature (T a) of 15 °C (T b ∼18 °C), whereas females only raised their heads. The responses were less pronounced at T a 10 °C. The first coordinated movement of possums along a branch was observed at a mean T b of 15.6 °C, and animals were even able to climb their prehensile tail when they reached a mean T b of 24.4 °C. Our study shows that hibernators can sense smoke and move at low T b. However, our data also illustrate that at T b ≤13 °C, C. nanus show decreased responsiveness and locomotor performance and highlight that prescribed burns during winter should be avoided on very cold days to allow torpid animals enough time to respond.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Choi I-H, Cho Y, Oh YK, Jung N-P, Shin H-C (1998) Behavior and muscle performance in heterothermic bats. Physiol Zool 71:257–266. doi:10.1086/515915
Engstrom RT (2010) First-order fire effects on animals: review and recommendations. Fire Ecol 6:115–130. doi:10.4996/fireecology.0601115
Geiser F (2007) Yearlong hibernation in a marsupial mammal. Naturwissenschaften 94:941–944. doi:10.1007/s00114-007-0274-7
Geiser F (2013) Hibernation. Curr Biol 23:R188–R193. doi:10.1016/j.cub.2013.01.062
Geiser F, Turbill C (2009) Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96:1235–1240. doi:10.1007/s00114-009-0583-0
Grafe TU, Döbler S, Linsenmair KE (2002) Frogs flee from the sound of fire. Proc Roy Soc B-Biol Sci 269:999–1003. doi:10.1098/rspb.2002.1974
Hanna E, Cardillo M (2014) Clarifying the relationship between torpor and anthropogenic extinction risk in mammals. J Zool 293:211–217. doi:10.1111/jzo.12136
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. doi:10.1002/bimj.200810425
Larkin JE, Heller HC (1996) Temperature sensitivity of sleep homeostasis during hibernation in the golden-mantled ground squirrel. Am J Physiol Regul Integr Comp Physiol 270:R777–R784
Larkin JE, Heller HC (1999) Sleep after arousal from hibernation is not homeostatically regulated. Am J Physiol 276:R522–R529
Luo J, Clarin B-M, Borissov IM, Siemers BM (2014) Are torpid bats immune to anthropogenic noise? J Exp Biol 217:1072–1078. doi:10.1242/jeb.092890
Menkhorst PW (1995) Eastern pygmy-possum. In: Menkhorst PW (ed) Mammals of Victoria: distribution, ecology and conservation Oxford University Press, Melbourne
Moritz MA, Parisien M-A, Batllori E, Krawchuk MA, Van Dorn J, Ganz DJ, Hayhoe K (2012) Climate change and disruptions to global fire activity. Ecosphere 3:art49. doi:10.1890/es11-00345.1
Mzilikazi N, Lovegrove BG, Ribble GO (2002) Exogenous passive heating during torpor arousal in free-ranging rock elephant shrews, Elephantulus myurus. Oecologia 133:307–314
Nowack J, Cooper CE, Geiser F (2016) Cool echidnas survive the fire. P Roy Soc B 283 doi:10.1098/rspb.2016.0382
NSW NPWS (2015) Threatened species list: Cercatetus nanus. http://www.environment.nsw.gov.au/threatenedspecies/. Accessed 20.11.15 2015
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) Linear and nonlinear mixed effects models
R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rojas AD, Körtner G, Geiser F (2010) Do implanted transmitters affect maximum running speed of two small marsupials? J Mammal 91:1360–1364. doi:10.1644/10-mamm-a-052.1
Rojas AD, Körtner G, Geiser F (2012) Cool running: locomotor performance at low body temperature in mammals. Biol Lett 8:868–870. doi:10.1098/rsbl.2012.0269
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926. doi:10.1111/brv.12137
Scesny AA, Robbins LW (2006) Detection of fire by eastern red bats (Lasiurus borealis): arousal from torpor. Doctoral dissertation, Missouri State University
Song X, Körtner G, Geiser F (1997) Thermal relations of metabolic rate reduction in a hibernating marsupial. Am J Physiol Regul Integr Comp Physiol 273:R2097–R2104
Speakman JR, Webb PI, Racey PA (1991) Effects of disturbance on the energy expenditure of hibernating bats. J Appl Ecol 28:1087–1104. doi:10.2307/2404227
Stawski C, Körtner G, Nowack J, Geiser F (2015a) The importance of mammalian torpor for survival in a post-fire landscape. Biol Letters 11 doi:10.1098/rsbl.2015.0134
Stawski C, Matthews JK, Körtner G, Geiser F (2015b) Physiological and behavioural responses of a small heterothermic mammal to fire stimuli. Physiol Behav 151:617–622. doi:10.1016/j.physbeh.2015.09.002
Tattersall GJ, Sinclair BJ, Withers PC, Fields PA, Seebacher F, Cooper CE, Maloney SK (2012) Coping with thermal challenges: physiological adaptations to environmental temperatures. In: Comprehensive physiology. John Wiley & Sons, Inc. doi:10.1002/cphy.c110055
Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc Roy Soc B-Biol Sci 278:3355–3363. doi:10.1098/rspb.2011.0190
Turner JM, Körtner G, Warnecke L, Geiser F (2012) Summer and winter torpor use by a free-ranging marsupial. Comp Biochem Physiol A 162:274–280. doi:10.1016/j.cbpa.2012.03.017
Wacker CB, Rojas AD, Geiser F (2012) The use of small subcutaneous transponders for quantifying thermal biology and torpor in small mammals. J Therm Biol 37:250–254. doi:10.1016/j.jtherbio.2011.11.007
Warnecke L, Geiser F (2010) The energetics of basking behaviour and torpor in a small marsupial exposed to simulated natural conditions. J Comp Physiol B 180:437–445. doi:10.1007/s00360-009-0417-6
Warnecke L, Turner J, Geiser F (2008) Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95:73–78. doi:10.1007/s00114-007-0293-4
Whelan RJ (1995) The ecology of fire. Cambridge University Press, United Kingdom
Wooden KM, Walsberg GE (2003) Body temperature and locomotor capacity in a heterothermic rodent. J Exp Biol 207:41–46
Wynn ML, Clemente C, Nasir AFAA, Wilson RS (2015) Running faster causes disaster: trade-offs between speed, manoeuvrability and motor control when running around corners in northern quolls (Dasyurus hallucatus). J Exp Biol 218:433–439. doi:10.1242/jeb.111682
We thank Arne Müller and Chris Wacker for the assistance in animal maintenance. The project was supported by grants from the German Academic Exchange Service and the A.F.W. Schimper Stiftung für ökologische Forschung to JN, a University of New England Postdoctoral Research Fellowship to CS, by the Australian Research Council and the University of New England to FG and by the French Ministry of Agriculture, Agrifood and Forestry and by the Region Auvergne (France) to MD.
Communicated by: Sven Thatje
About this article
Cite this article
Nowack, J., Delesalle, M., Stawski, C. et al. Can hibernators sense and evade fires? Olfactory acuity and locomotor performance during deep torpor. Sci Nat 103, 73 (2016). https://doi.org/10.1007/s00114-016-1396-6
- Cercartetus nanus
- Sensory perception